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      Coincidence of pheromone and plant odor leads to sensory plasticity in the heliothine olfactory system

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          Abstract

          Male moths possess a highly specialized olfactory system comprised of two segregated sub-arrangements dedicated to processing information about plant odors and pheromones, respectively. Communication between these two sub-systems has been described at the peripheral level, but relatively little is known about putative interactions at subsequent synaptic relays. The male moth faces the challenge of seeking out the conspecific female in a highly dynamic odor world. The female-produced pheromone blend, which is a limited resource serving as guidance for the male, will reach his antennae in intermittent pockets of odor filaments mixed with volatiles from various plants. In the present study we performed calcium imaging for measuring odor-evoked responses in the uni-glomerular antennal-lobe projection neurons (analog to mitral cells in the vertebrate olfactory bulb) of Helicoverpa armigera. In order to investigate putative interactions between the two sub-systems tuned to plant volatiles and pheromones, respectively, we performed repeated stimulations with a selection of biologically relevant odors. We found that paired stimulation with a plant odor and the pheromone led to suppressed responses in both sub-systems as compared to those evoked during initial stimulation including application of each odor stimulus alone. The fact that the suppression persisted also after pairing, indicates the existence of a Hebbian-like plasticity in the primary olfactory center established by temporal pairing of the two odor stimulation categories.

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          Most cited references42

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          Mechanisms of olfactory discrimination: converging evidence for common principles across phyla.

          Olfaction begins with the transduction of the information carried by odor molecules into electrical signals in sensory neurons. The activation of different subsets of sensory neurons to different degrees is the basis for neural encoding and further processing of the odor information by higher centers in the olfactory pathway. Recent evidence has converged on a set of transduction mechanisms, involving G-protein-coupled second-messenger systems, and neural processing mechanisms, involving modules called glomeruli, that appear to be adapted for the requirements of different species. The evidence is highlighted in this review by focusing on studies in selected vertebrates and in insects and crustaceans among invertebrates. The findings support the hypothesis that olfactory transduction and neural processing in the peripheral olfactory pathway involve basic mechanisms that are universal across most species in most phyla.
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            Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study.

            The primary olfactory brain center, the antennal lobe (AL) in insects or the olfactory bulb in vertebrates, is a notable example of a neural network for sensory processing. While physiological properties of the input, the olfactory receptor neurons, have become clearer, the operation of the network itself remains cryptic. Therefore we measured spatio-temporal odor-response patterns in the output neurons of the olfactory glomeruli using optical imaging in the honeybee Apis mellifera. We mapped these responses to identified glomeruli, which are the structural and functional units of the AL. Each odor evoked a complex spatio-temporal activity pattern of excited and inhibited glomeruli. These properties were odor- and glomerulus-specific and were conserved across individuals. We compared the spatial pattern of excited glomeruli to previously published signals, which derived mainly from the receptor neurons, and found that they appeared more confined, showing that inhibitory connections enhance the contrast between glomeruli in the AL. To investigate the underlying mechanisms, we applied GABA and the GABA-receptor antagonist picrotoxin (PTX). The results show the presence of two separate inhibitory networks: one is GABAergic and modulates overall AL activity, the other is PTX-insensitive and glomerulus-specific. Inhibitory connections of the latter network selectively inhibit glomeruli with overlapping response profiles, in a way akin to "lateral" inhibition in other sensory systems. Selectively inhibited glomeruli need not be spatial neighbors. The net result is a globally modulated, contrast-enhanced and predictable representation of odors in the olfactory output neurons.
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              Processing of odor mixtures in the Drosophila antennal lobe reveals both global inhibition and glomerulus-specific interactions.

              To understand how odor information is represented and processed in the antennal lobe (AL) of Drosophila melanogaster, we have optically recorded glomerular calcium responses to single odors and odor mixtures from olfactory sensory neurons (OSNs) and projection neurons (PNs). Odor mixtures offer a good tool to analyze odor processing because experimental results can be tested against clear predictions. At the level of the OSNs, the representation of odor mixtures could be predicted from the response patterns of the components in most cases. PN responses to mixtures, however, provide evidences of interglomerular inhibition. Application of picrotoxin (PTX), an antagonist of GABA(A)-like receptors, enhanced odor responses, modified their temporal course, and eliminated mixture suppression at the PN level. Our results can be best explained by postulating the existence of at least two local networks in the fly AL: a glomerulus specific network, which includes excitatory and inhibitory connections and a PTX sensitive inhibitory global network that acts on all glomeruli with proportional strength to the global AL input.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                3 May 2017
                2017
                : 12
                : 5
                : e0175513
                Affiliations
                [1 ]Norwegian University of Science and Technology (NTNU), Department of Psychology, Trondheim, Norway
                [2 ]Universität Konstanz Fachbereich Biologie, Konstanz, Germany
                INRA-UPMC, FRANCE
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: NHK EI BGB CGG.

                • Data curation: NHK.

                • Formal analysis: NHK.

                • Investigation: NHK EI.

                • Methodology: NHK EI CGG BGB.

                • Project administration: BGB.

                • Resources: BGB EI NHK.

                • Software: NHK.

                • Supervision: BGB CGG.

                • Validation: BGB NHK CGG.

                • Visualization: NHK.

                • Writing – original draft: BGB EI NHK CGG.

                • Writing – review & editing: BGB EI NHK CGG.

                Author information
                http://orcid.org/0000-0002-2125-6940
                Article
                PONE-D-16-49200
                10.1371/journal.pone.0175513
                5414983
                28467500
                0a33a089-7466-41f6-9d30-b1113554c0ad
                © 2017 Ian et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 13 December 2016
                : 27 March 2017
                Page count
                Figures: 8, Tables: 0, Pages: 16
                Funding
                The authors received no specific funding for this work.
                Categories
                Research Article
                Biology and Life Sciences
                Biochemistry
                Pheromones
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Moths and Butterflies
                Biology and Life Sciences
                Organisms
                Plants
                Flowering Plants
                Sunflower
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Neurons
                Biology and Life Sciences
                Neuroscience
                Cellular Neuroscience
                Neurons
                Biology and Life Sciences
                Zoology
                Entomology
                Insect Pheromones
                Biology and Life Sciences
                Biochemistry
                Pheromones
                Insect Pheromones
                Research and Analysis Methods
                Imaging Techniques
                Neuroimaging
                Calcium Imaging
                Biology and Life Sciences
                Neuroscience
                Neuroimaging
                Calcium Imaging
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Flower Anatomy
                Calyx
                Biology and Life Sciences
                Neuroscience
                Cellular Neuroscience
                Synaptic Plasticity
                Biology and Life Sciences
                Neuroscience
                Developmental Neuroscience
                Synaptic Plasticity
                Custom metadata
                All relevant data are within the manuscript and its Supporting Information files. Imaging raw data files are available at: 10.6084/m9.figshare.4810420.

                Uncategorized
                Uncategorized

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